Body mass and growth rates predict protein intake across animals

  1. Stav Talal
  2. Jon F. Harrison
  3. Ruth Farington
  4. Jacob P. Youngblood
  5. Hector E. Medina
  6. Rick Overson
  7. Arianne J. Cease

  • Curated by eLife

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    How and why nutritional requirements change over development and differ between species are significant questions with wide-ranging implications spanning ecology to health. In this manuscript, Talal et al. set out to address these questions in laboratory and field experiments with grasshoppers and in a comparative analysis of different species. The laboratory experiments are convincing but the field and comparative aspects are not sufficiently well developed. In general, the study offers some evidence of a universal shift from high protein to high carbohydrate intake during ontogeny in animals, but the methods are not clear and/or appropriate to support the goals and conclusions of the manuscript as it is.

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Abstract

Organisms require dietary macronutrients in specific ratios to maximize performance, and variation in macronutrient requirements plays a central role in niche determination. Although it is well-recognized that development and body size can have strong and predictable effects on many aspects of organismal function, we lack a predictive understanding of ontogenetic or scaling effects on macronutrient intake. We determined protein and carbohydrate intake throughout development on lab populations of locusts and tested whether lab responses can predict results for field populations. Self-selected protein:carbohydrate targets declined dramatically through ontogeny, due primarily to declines in mass-specific protein consumption rates which were highly correlated with declines in specific growth rates. Importantly, lab results for protein consumption rates predicted results for field-collected locusts. However, field locusts consumed nearly double the carbohydrate, likely due to higher activity and metabolic rates. Combining our results with the available data for animals, both across species and during ontogeny, protein consumption scaled predictably and hypometrically, demonstrating a new scaling rule key for understanding nutritional ecology.

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  1. eLife

    Author response:

    Reviewer #1 (Public Review):

    The authors tested the hypothesis that protein consumption decreases with decreasing mass-specific growth during development. This hypothesis is firmly grounded in the logical premise that as animals progress from periods of reduced activity and rapid growth to phases of increased activity and reduced mass-specific growth during their development, they are likely to adjust their nutrient intake, reducing protein and increasing carbohydrate consumption accordingly. The authors tested their hypothesis using the South American locust Schistocerca cancellata, combining field observations with laboratory experiments. This approach allowed them to discern how variations in activity history and metabolism between field- and laboratory-raised locusts influenced their nutrient requirements.

    Their findings, indeed reveal the predicted shift from high protein: carbohydrate consumption to lower protein: carbohydrate intake from the first instar to adult locust - a decline that strongly correlated with a decrease in mass-specific growth rate. Their comparison between field- and laboratory-raised locusts, showed that protein demand was not different, however, carbohydrate consumption rate was >50% higher in the field locusts. These results add depth and significance to the study, shedding light on how environmental factors influence nutrient requirements. What truly amplifies the strength and novelty of the authors' hypothesis is their anticipation that this observed trend in Schistocerca cancellata could extend to all animals. This anticipation is rooted in the expectation that growth rates scale hypometrically across various body sizes and developmental stages, introducing a universal dimension to their findings that holds great promise for broader ecological and evolutionary understanding.

    However, while the study is commendable in its methodology and core findings, there is room for improvement in clarifying the implications of the results. The current lack of clarity is evident in the somewhat shallow questions outlined in lines 358 to 363. For instance, the practice of administering age-specific diets has been commonplace in human and livestock management for ages. Thus, its continued utility may not be the most stimulating question. Instead, a more thought-provoking inquiry might delve into whether variations in global protein availability play a pivotal role in driving niche specialization and the biogeography of animal body sizes and ontogeny, especially considering the potential impacts of climate change. Such inquiries would further elevate the significance of the author's work and its broader implications in the field.

    Thanks for the suggestions. We have added additional sentences to the discussion regarding how size affects protein:carbohydrate consumption may affect physiology and ecology of animals.

    Reviewer #2 (Public Review):

    How and why nutritional requirements and intake targets change over development and differ between species are significant questions with wide-ranging implications spanning ecology to health. In this manuscript, Talal et al. set out to address these questions in laboratory and field experiments with grasshoppers and in a comparative analysis of different species.

    The authors conclude that the target intake of protein to non-protein energy (in this case carbohydrate) (P:C) falls over developmental stages and that this occurs because of a decline in mass-specific intake of protein whereas mass-specific carbohydrate intake remains more constant. The decrease in mass-specific protein consumption rate is tightly correlated with a decline in specific growth rate. Hence, protein consumption directly reflects requirements for growth, with hypometric scaling of protein intake serving as a useful relationship in nutritional ecology.

    The laboratory experiments on the locust, Schistocerca cancellata, provide an elegant dataset in which different instars have been provided with one of two nutritionally complementary food pairings differing in protein to carbohydrate (P: C) content, and their self-selected protein to carbohydrate "intake target" measured.

    These lab locust results were then compared with independently collected field data for late instar nymphs of the same locust species, and the conclusion is drawn that field insects ingested similar protein but 50-90% more carbohydrate (with only 23% increased mass-specific resting oxygen consumption rates). Numerous uncontrolled variables between the lab and field studies make meaningful conclusions difficult to draw from this observation.

    Thank you for this comment. We have revised the text to better explain that very few studies have directly compared lab and field intake target data, and that our goal was to test whether lab intake targets predicted those for field-collected animals. We have also revised the discussion to describe the many possible reasons that intake targets for field-collected animals may diverge from those of lab-reared locust.

    A graph is then provided showing comparative data across a selection of species, making the case that protein consumption scales similarly both developmentally and across taxa. Questions need to be addressed for this to be convincing, including which criteria were used to select the examples in the graph and how comprehensively do these represent the available literature.

    We now provide further data in the methods on our literature search methods.

    Reviewer #3 (Public Review):

    The main goal of this study was to test how and why the intake of two important macronutrients ‒protein and carbon‒ often changes with ontogeny and body size. To do this, authors examined protein and carbon intake in a locusts lab population, across each instar and adult stages. Then, authors examined how the optimal balance of carbon and protein intake in a wild locusts population corresponded to that observed in the laboratory population. Results of these experiments showed that with ontogenic growth, locust decreased protein while increasing carbohydrate intake. Authors concluded that such decrease in the protein: carbohydrate intake may result from reductions in specific growth rates (growth within each instar). The protein: carbohydrate intake in the lab population appeared to be consistent with that observed in a wild locust population. Finally, authors combined their data with that from the literature to examine how protein intake scales with body mass throughout development, within and across different species.

    Strengths:

    To determine how locusts balance protein: carbohydrate intake, authors applied the Geometric Framework (GF) of nutrition, which is a powerful approach for studying effects of nutrition and understanding the rules of compromise associated with balancing dietary unbalances.

    Captivity can change behavior and physiology of most organisms, making it difficult to establish the relevance of laboratory experiments to what happens in the real world. A strength of this paper is that it compares behavior/physiology of lab vs. wild locusts. Finally, this study takes a step further by proposing a new scaling rule based on this study's results and data from the literature on various species.

    Weaknesses:

    Although the paper has strengths, there seems to be several methodological issues that obscure the interpretation/conclusions presented in the manuscript.

    It appears that authors are not actually estimating "Intake Targets", as stated throughout the manuscript. According to the geometric framework, the intake target (IT) is estimated as the point in the nutritional landscape under which performance/fitness is optimized. The geometric framework also predicts that animals can reach their intake targets by feeding selectivity when given a choice of diets that differ in nutrient amounts, which is what authors did here. However, because the relationship between fitness/performance with diet was not established, in the choice experiments authors seem to be assuming (but not testing) that locusts are reaching their intake target.

    The reviewer is correct that we have not tested whether the intake target selected by each instar maximizes growth or some other measure of fitness. This is a nontrivial task, as there are many possible indices of fitness for juvenile instars, including growth rate, developmental time, resistance to disease/stress, as well as effects on adult reproduction. We use intake target as defined by Raubenheimer and Simpson (2018), “the intake target (IT) is a geometric representation of the nutrient mixture that the regulatory systems target through foraging and feeding.” As we explain above, we followed the protocols used by most investigators to measure intake targets, including for many papers locusts.

    You estimated a mass-specific protein intake for each instar. It is not clear why mass-specific intake and not just intake of protein was used for analysis. While mass (or size) of an individual may influence food consumption, it seems like authors calculated mass-specific consumption using each instar's final mass, which would make mass a result of protein consumption (and not the opposite). Importantly, the comparison between mass-specific protein consumption and specific growth rate may be problematic, as both variables seem to be estimated using final mass.

    Thank you for this important comment. We agree and therefore, we changed figure 2 and the related analyses, using protein consumption rate corrected for initial rather than final mass.

  2. eLife

    eLife assessment

    How and why nutritional requirements change over development and differ between species are significant questions with wide-ranging implications spanning ecology to health. In this manuscript, Talal et al. set out to address these questions in laboratory and field experiments with grasshoppers and in a comparative analysis of different species. The laboratory experiments are convincing but the field and comparative aspects are not sufficiently well developed. In general, the study offers some evidence of a universal shift from high protein to high carbohydrate intake during ontogeny in animals, but the methods are not clear and/or appropriate to support the goals and conclusions of the manuscript as it is.

  3. eLife

    Reviewer #1 (Public Review):

    The authors tested the hypothesis that protein consumption decreases with decreasing mass-specific growth during development. This hypothesis is firmly grounded in the logical premise that as animals progress from periods of reduced activity and rapid growth to phases of increased activity and reduced mass-specific growth during their development, they are likely to adjust their nutrient intake, reducing protein and increasing carbohydrate consumption accordingly. The authors tested their hypothesis using the South American locust Schistocerca cancellata, combining field observations with laboratory experiments. This approach allowed them to discern how variations in activity history and metabolism between field- and laboratory-raised locusts influenced their nutrient requirements.
    Their findings, indeed reveal the predicted shift from high protein: carbohydrate consumption to lower protein: carbohydrate intake from the first instar to adult locust - a decline that strongly correlated with a decrease in mass-specific growth rate. Their comparison between field- and laboratory-raised locusts, showed that protein demand was not different, however, carbohydrate consumption rate was >50% higher in the field locusts. These results add depth and significance to the study, shedding light on how environmental factors influence nutrient requirements.
    What truly amplifies the strength and novelty of the authors' hypothesis is their anticipation that this observed trend in Schistocerca cancellata could extend to all animals. This anticipation is rooted in the expectation that growth rates scale hypometrically across various body sizes and developmental stages, introducing a universal dimension to their findings that holds great promise for broader ecological and evolutionary understanding.
    However, while the study is commendable in its methodology and core findings, there is room for improvement in clarifying the implications of the results. The current lack of clarity is evident in the somewhat shallow questions outlined in lines 358 to 363. For instance, the practice of administering age-specific diets has been commonplace in human and livestock management for ages. Thus, its continued utility may not be the most stimulating question. Instead, a more thought-provoking inquiry might delve into whether variations in global protein availability play a pivotal role in driving niche specialization and the biogeography of animal body sizes and ontogeny, especially considering the potential impacts of climate change. Such inquiries would further elevate the significance of the author's work and its broader implications in the field.

  4. eLife

    Reviewer #2 (Public Review):

    How and why nutritional requirements and intake targets change over development and differ between species are significant questions with wide-ranging implications spanning ecology to health. In this manuscript, Talal et al. set out to address these questions in laboratory and field experiments with grasshoppers and in a comparative analysis of different species.

    The authors conclude that the target intake of protein to non-protein energy (in this case carbohydrate) (P:C) falls over developmental stages and that this occurs because of a decline in mass-specific intake of protein whereas mass-specific carbohydrate intake remains more constant. The decrease in mass-specific protein consumption rate is tightly correlated with a decline in specific growth rate. Hence, protein consumption directly reflects requirements for growth, with hypometric scaling of protein intake serving as a useful relationship in nutritional ecology.

    The laboratory experiments on the locust, Schistocerca cancellata, provide an elegant dataset in which different instars have been provided with one of two nutritionally complementary food pairings differing in protein to carbohydrate (P: C) content, and their self-selected protein to carbohydrate "intake target" measured.

    These lab locust results were then compared with independently collected field data for late instar nymphs of the same locust species, and the conclusion is drawn that field insects ingested similar protein but 50-90% more carbohydrate (with only 23% increased mass-specific resting oxygen consumption rates). Numerous uncontrolled variables between the lab and field studies make meaningful conclusions difficult to draw from this observation.

    A graph is then provided showing comparative data across a selection of species, making the case that protein consumption scales similarly both developmentally and across taxa. Questions need to be addressed for this to be convincing, including which criteria were used to select the examples in the graph and how comprehensively do these represent the available literature.

  5. eLife

    Reviewer #3 (Public Review):

    The main goal of this study was to test how and why the intake of two important macronutrients ‒protein and carbon‒ often changes with ontogeny and body size. To do this, authors examined protein and carbon intake in a locusts lab population, across each instar and adult stages. Then, authors examined how the optimal balance of carbon and protein intake in a wild locusts population corresponded to that observed in the laboratory population. Results of these experiments showed that with ontogenic growth, locust decreased protein while increasing carbohydrate intake. Authors concluded that such decrease in the protein: carbohydrate intake may result from reductions in specific growth rates (growth within each instar). The protein: carbohydrate intake in the lab population appeared to be consistent with that observed in a wild locust population. Finally, authors combined their data with that from the literature to examine how protein intake scales with body mass throughout development, within and across different species.

    Strengths:
    To determine how locusts balance protein: carbohydrate intake, authors applied the Geometric Framework (GF) of nutrition, which is a powerful approach for studying effects of nutrition and understanding the rules of compromise associated with balancing dietary unbalances.

    Captivity can change behavior and physiology of most organisms, making it difficult to establish the relevance of laboratory experiments to what happens in the real world. A strength of this paper is that it compares behavior/physiology of lab vs. wild locusts. Finally, this study takes a step further by proposing a new scaling rule based on this study's results and data from the literature on various species.

    Weaknesses:
    Although the paper has strengths, there seems to be several methodological issues that obscure the interpretation/conclusions presented in the manuscript.
    It appears that authors are not actually estimating "Intake Targets", as stated throughout the manuscript. According to the geometric framework, the intake target (IT) is estimated as the point in the nutritional landscape under which performance/fitness is optimized. The geometric framework also predicts that animals can reach their intake targets by feeding selectivity when given a choice of diets that differ in nutrient amounts, which is what authors did here. However, because the relationship between fitness/performance with diet was not established, in the choice experiments authors seem to be assuming (but not testing) that locusts are reaching their intake target.

    You estimated a mass-specific protein intake for each instar. It is not clear why mass-specific intake and not just intake of protein was used for analysis. While mass (or size) of an individual may influence food consumption, it seems like authors calculated mass-specific consumption using each instar's final mass, which would make mass a result of protein consumption (and not the opposite). Importantly, the comparison between mass-specific protein consumption and specific growth rate may be problematic, as both variables seem to be estimated using final mass.

  6. Version published to 10.1101/2023.06.20.545784v1 on bioRxiv